FILE: <bc-10.htm> GENERAL INDEX [Navigate to MAIN MENU ]
EXTRANUCLEAR EVENTS INFLUENCING BEHAVIOR
AND
FECUNDITY IN PARASITOIDS AND OTHER ANIMALS
----Please CLICK on desired
underlined categories [to search for Subject Matter,
depress Ctrl/F ]:
Extranuclear
influences on behavior
Direct
Effects of the Cytoplasmic Genome
Chemical Substances Affecting Behavior
Muscidifurax
Parasitoid Complex
[ Please refer
also to Selected
Reviews #1, #2
& Detailed Research ]
|
Extranuclear influences on behavior involving
cytoplasmic entities are well known among both prokaryotes and eukaryotes
(Beale & Knowles 1978, Cosmides & Tooby 1981, Goodenough 1984, Levine
1973, Sager & Ramanis 1963, Sonneborn 1959), but the subsequent
incorporation of an extranuclear expression into the nuclear genome
apparently has not been found. Extranuclear factors in the form of
microorganisms (e.g., viruses, bacteria, spiroplasmas) can alter sex ratios
in parasitoids by selectively killing developing males or females (Skinner
1982, 1985; Werren et al. 1981, 1986), may confer resistance to host
encapsulation (Krell & Stoltz 1979, Stoltz & Vinson 1977, Stoltz et
al. 1976, Vinson & Stoltz 1986), and affect sex ratios in Drosophila
(Poulson & Sakaguchi 1961), and are passed on to succeeding generations.
Cosmides and Tooby (1981) recently reviewed how cytoplasmic genes control
such characters as allocation of reproductive effort in hermaphrodites, sex
ratios of offspring (Williamson & Poulson 1979), organism size (Faulkner
& Arlett 1964), growth rate, colony size, rate of senescence (Smith &
Rubenstein 1973), competitive ability (Preer et al. 1974), drug resistance in
bacteria, protozoans, fungi, and mammals (Beale & Knowles 1978), and
rates of recombination among nuclear genes (Thoday & Boam 1956). Oishi et
al. (1984) explained how two kinds of microorganisms (spiroplasma and virus)
may interact to modify expressions of the sex-ratio factor in Drosophila.
Stoltz & Vinson (1979) have found viruses in the calyx epithelial cells
of endoparasitoids. Fleming & Summers (1986) found them also in the lumen
of the oviduct. These viruses were passed from parent to offspring, males
being able to transmit viral DNA to females with whom they mated (Stoltz et
al. 1986). The direct effects of the cytoplasmic
genome on the nuclear genome has been hypothesized (Cosmides &
Tooby 1981), but not demonstrated. However, the extrachromosomal genetic
system can be influenced by the chromosomal system (Levine 1973).
Microorganisms implicated in inheritance have been known to cause illness and
death in male Drosophila (Leventhal 1968). Chemical substances affect behavior of insects
following mating. Reports include a lepidopteran (Webster & Carde 1984),
and ichneumon wasp Venturia (Nemeritis) canescens
(Gravenhorst) (where heneicosane was involved) (Mudd et al. 1982); and the
dipteran Drosophila, involving enzymes (Mane et al. 1983, Richmond
& Senior 1981). Prostaglandins, derivatives of certain polyunsaturated
fatty acids, alter egg laying behavior in crickets (Stanley-Samuelson &
Loher 1986). It has been suggested than an influence on the chemosensory responsiveness
of an individual by chemical cues derived from its parents would be hard to
distinguish from a genetic effect (Corbet 1985). Microorganisms involved in the production of
thelytoky have been identified molecularly by Stouthamer et al. (1993). They
comment that inherited microorganisms are widespread in insects, having been
implicated as causes of female parthenogenesis and cytoplasmic
incompatibility. Normal sexual reproduction can be restored by treatment with
antibiotics. Sequence analysis of the DNA encoding 16S ribosomal RNA show
that cytoplasmic incompatibility bacteria from diverse insect taxa are
closely related, sharing 95% sequence similarity. They belong to the alpha
subdivision of Proteobacteria. Stouthamer et al. (1993) show that parthenogenesis-associated
bacteria from parasitoid Hymenoptera fall into this bacterial group, having
up to 99% sequence similarity to some incompatibility microorganisms. Both
incompatibility and parthenogenesis microorganisms alter host chromosome
behavior during early mitotic division in the egg. Incompatibility bacteria
act by interfering with paternal chromosome incorporation in fertilized eggs,
while parthenogenesis bacteria prevent segregation of chromosomes in
unfertilized eggs. These traits are adaptive for the microorganisms. Judging
from their sequence similarities, Stouthamer et al. (1993) concluded that
parthenogenesis bacteria and cytoplasmic incompatibility bacteria form a
monophyletic group of microorganisms that specialize in manipulating chromosome
behavior and insect reproduction. Research on the genus Muscidifurax (see Research) has uncovered
a polygenic system controlling rates of larval cannibalism and therefore
reproductive success. The genes involved are able to cause partial expression
of the traits they govern shortly after insemination and before being
inherited by the progeny. Extranuclear phases prior to chromosomal
inheritance may involve microorganisms and/or enzymes present in hymenopteran
seminal fluid. The ability to
change expression of a quantitative character immediately after mating,
either positively or negatively, challenges accepted views of polygenic loci,
and it may be that such loci are not in fact inherited, but rather another group
of genes which have the capability to switch on or off the
loci. Such genes may influence DNA methylation of the loci controlling
oviposition behavior, as shown for other organisms (). All polygenic loci may
be perpetually present for a given quantitative trait in all individuals of
both Muscidifurax raptorellus races, but they are either
activated or inactivated by substances under the control of another group of
genes (Legner 1993 ). Evolution in the
Muscidifurax system is theoretically accelerated by allowing natural
selection for nonlethal undesirable and desirable characteristics to begin to
act in the parental generation. Traits which are detrimental to the
population might thus be more prone to elimination and beneficial ones may be
expressed in the mother before the appearance of her active progeny. If a
similar genetic system occurs more generally in Hymenoptera, it might account
partially for the rapid evolution thought to occur in certain groups of Hymenoptera.
The ability of male Hymenoptera to activate heritable behavior in females
with whom they mate has practical significance in biological control. Greater
importance may be placed on liberated males during mass release strategies
that seek to accelerate and increase the magnitude of parasitism, because it
is possible to convey certain desirable strain characteristics directly to
unmated females already resident in the environment. This subject will be
treated in greater detail in a subsequent section on arrhenotoky. Further
studies in 1995 by Stouthamer et al. (unpublished) have shown the involvement
of larval cannibalism and much greater complexities in this species'
reproduction. An account may be found in <aggress.htm>. [ Please refer also to Related Research ] Exercise 10.1. How may you
distinguish behavior that is regulated by extranuclear factors from that
regulated by genetic factors? Exercise 10.2. Name the kinds
of organisms that have been implicated in triggering extranuclear responses
in animals. Exercise 10.3. Could
extranuclear factors be used to control behavior in insects? REFERENCES: [ Additional references may be
found at MELVYL
Library ] Ayala, F. J. & J. A. Kiger, Jr.
1984. Modern Genetics, 2nd ed. The Benjamin/Cummings Publ. Co., Inc. Menlo
Park, CA. 923 p. Beale, G. & J. Knowles. 1978.
Extranuclear Genetics. Edward Arnold, London. 142 p. Bellows, T. S., Jr. & T. W. Fisher,
(eds) 1999. Handbook of Biological Control: Principles and Applications.
Academic Press, San Diego, CA. 1046 p. Bownes, M. & L. Partridge. 1987.
Transfer of molecules from ejaculate to females in Drosophila melanogaster
and Drosophila pseudoobscura. J. Insect Physiol. 33: 941-47.
Bull, J. J. 1983. Evolution of Sex Determining Mechanisms. The Benjamin/Cummings
Publ. Co., Inc., Menlo Park, CA. 316 p. Cosmides, L. M. & J. Tooby. 1981.
Cytoplasmatic inheritance and intragenomic conflict. J. Theor. Biol. 89:
83-129. Corbet, S. A. 1985. Insect chemosensory
responses: a chemical legacy hypothesis. Ecol. Ent. 10: 143-53. 264. Etzel, L. K. & E. F. Legner. 1999.
Culture and Colonization. In: T. W. Fisher & T. S. Bellows, Jr. (eds.), Chapter 15, p.
125-197, Handbook of Biological
Control: Principles and
Applications. Academic Press, San
Diego, CA 1046 p. Faulkner, B. M. & C. F. Arlett.
1964. The "minute" cytoplasmic variant of Aspergillus nidulans.
Heredity 19: 63-73. Fleming, J. G. W. & M. D. Summers.
1986. Campoletis sonorensis endoparasitic wasps contain forms
of C. sonorensis virus DNA suggestive of integrated and
extrachromosomal polydnavirus DNAs. J. Virol. 57: 552-62. Goodenough, U. 1984. Genetics, 3d. ed.
Saunders College Publ., Philadelphia/New York. 894 p. Gordh, G. 1975. Some evolutionary trends
in the Chalcidoidea (Hymenoptera) with particular reference to host
preference. J. New York Ent. Soc. 83: 279-80. Gordh, G. 1979. Catalog of Hymenoptera
in America north of Mexico. Smithsonian Inst. Press, Vol. I, pp. 743-48. Gwynne, D. T. 1984. Courtship feeding
increases female reproductive success in bush crickets. Nature 307: 361-63. Krell, P. J. & D. B. Stoltz. 1979.
Unusual baculovirus of the parasitoid wasp Apanteles melanoscelus:
isolation and preliminary characterization. J. Virol. 29: 1118-30. 228. Legner, E. F. 1986. Breeding superior
parasitoids of Diptera using a novel extranuclear inheritance mechanism. Proc. Calif. Mosq. & Vector Contr. Assoc., Inc.
44: 156-159. 233. Legner, E. F. 1987. Inheritance of
gregarious and solitary oviposition in Muscidifurax
raptorellus Kogan & Legner
(Hymenoptera: Pteromalidae). Canad. Entomol. 119(9): 791-808. 259. Legner, E. F. 1993. Theory for
quantitative inheritance of behavior in a protelean parasitoid, Muscidifurax raptorellus (Hymenoptera: Pteromalidae). European J. Ent. 90: 11-21. Leslie, T. F. 1984. A
"sex-ratio" condition in Oncopeltus fasciatus. J.
Heredity 75: 260-64. Levanthal, E. 1968. The sex ratio in Drosophila
bifasciata; its experimental transmission. J. Inv. Path. 11: 170-83. Levine, L. 1973. Biology of the Gene.
The C.V. Mosby Co., St. Louis. 358 p. Malogolowkin, C. 1959. Temperature
effects on maternally inherited "sex-ratio" condition. Amer. Nat.
93: 365-68. Mane, S. D., L. Tompkins & R. C.
Richmond. 1983. Male esterase 6 catalyzes the synthesis of a sex pheromone in
Drosophila melanogaster females. Science 222: 419-21. Mudd, A. R., C. Fisher & M. C.
Smith. 1982. Volatile hydrocarbons in the Dufour's gland of the parasite Nemeritis
canescens (Grav.) (Hymenoptera: Ichneumonidae). J. Chem. Ecol. 8:
1035-42. Oishi, K., D. F. Poulsen & D. L.
Williamson. 1984. Virus-mediated change in clumping properties of Drosophila
SR spiroplasmas. Curr. Microbiology 10: 153-58. Poulson, D. F. & B. Sakaguchi. 1961.
Nature of the "sex ratio" agent in Drosophila. Science 133:
1489-90. Preer, J. R., L. B. Preer & A.
Jurand. 1974. Kappa and other endosymbionts in Paramecium aurelia.
Bact. Rev. 38: 113-63. Richmond, R. C. & A. Senior. 1981.
Esterase 6 (EC 3.1.1.1.) of Drosophila melanogaster: kinetics
of transfer to females, decay in females and male recovery. J. Insect
Physiol. 27: 849-54. Sager, R. & Z. Ramanis. 1963. The
particulate nature of nonchromosomal genes in Chlamydomonas. Proc.
Nat. Acad. Sci. U. S. A. 50: 260-68. Skinner, S. W. 1982. Maternally
inherited sex ratio in the parasitoid wasp Nasonia vitripennis.
Science 215: 1133-34. Skinner, S. W. 1985. Son-killer: a third
extrachromosomal factor affecting the sex-ratio. Genetics 109: 745-59. Smith, J. R. & I. Rubenstein. 1973.
The development of 'senescence' in Podospora anserina. J. Gen.
Microbiol. 76: 283-96. Sonneborn, T. M. 1959. Kappa and related
particles in Paramecium. Adv. Virus Res. 6: 229-356. Stanley-Samuelson, D. W. & W. Loher.
1986. Prostaglandins in insect reproduction. Ann. Ent. Soc. Amer. 79: 841-53. Steele, R. H. 1986. Courtship feeding in
Drosophila subobscura I. The nutritional significance of
courtship feeding. Anim. Behav. 34: 1987-98. Stoltz, D. B. & S. B. Vinson. 1977.
Baculovirus-like particles in the reproductive tracts of female parasitoid
wasp II: The genus Apanteles. Canad. J. Microbiol. 23: 28-37. Stoltz, D. B. & S. B. Vinson. 1979.
Viruses and parasitism in insects. Adv. Virus Res. 24: 125-71. Stoltz, D. B., S. B. Vinson & E. A.
Mackinnon. 1976. Baculovirus-like particles in the reproductive tracts of
female parasitoid wasps. Canad. J. Microbiol. 22: 1013-23. Stoltz, D. B., D. Guzo & D. Cook.
1986. Studies on polydnavirus transmission. Virology 155: 120-31. Stouthamer, R., J. A. J. Breeuwer, R. F.
Luck & J. H. Werren. 1993. Molecular identification of microorganisms
associated with parthenogenesis. Nature 361: 66-8. 2003. Stouthamer, Richard,, Patrycja
Strlppentow, Ingrld Langhout and E. Fred Legner. 2003. Genetics of
solitary and gregarious emergence in
the parasitoid wasp Muscidifurax raptorellus: paternal modification of larval aggression. (in process) Thoday, J. M. & T. B. Boam. 1956. A
possible effect of the cytoplasm recombination in Drosophila melanogaster.
J. Genet. 54: 456-61. Vinson, S. B. & D. B. Stoltz. 1986.
Cross-protection experiments with two parasitoid (Hymenoptera: Ichneumonidae)
viruses. Ann. Ent. Soc. Amer. 79: 216-18. Webster, R. P. & R. T. Carde. 1984.
The effects of mating, exogenous juvenile hormone and a juvenile hormone
analogue on pheromone titre, calling and oviposition in the omnivorous
leafroller moth (Platynota stultana). J. Insect Physiol. 30:
113-18. Werren, J. H., S. W. Skinner & E. L.
Charnov. 1981. Paternal inheritance of a daughterless sex ratio factor.
Nature 293: 467-68. Werren, J. H., S. W. Skinner & A. M.
Huger. 1986. Male-killing bacteria in a parasitic wasp. Science 231: 990-92. Williamson, D. L.
& D. F. Poulson. 1979. Sex ratio organisms (Spiroplasmas) of Drosophila.
The Mycoplasmas, Vol. 3: 175-208. |